Geographical patterns of adaptation within a species' range: interactions between drift and gene flow

We use individual-based stochastic simulations and analytical deterministic predictions to investigate the interaction between drift, natural selection and gene flow on the patterns of local adaptation across a fragmented species' range under clinally varying selection. Migration between populations follows a stepping-stone pattern and density decreases from the centre to the periphery of the range. Increased migration worsens gene swamping in small marginal populations but mitigates the effect of drift by replenishing genetic variance and helping purge deleterious mutations. Contrary to the deterministic prediction that increased connectivity within the range always inhibits local adaptation, simulations show that low intermediate migration rates improve fitness in marginal populations and attenuate fitness heterogeneity across the range. Such migration rates are optimal in that they maximize the total mean fitness at the scale of the range. Optimal migration rates increase with shallower environmental gradients, smaller marginal populations and higher mutation rates affecting fitness.     

Limits to evolution at range margins: when and why does adaptation fail?

What stops populations expanding into new territory beyond the edge of a range margin? Recent models addressing this problem have brought together population genetics and population ecology, and some have included interactions among species at range edges. Here, we review these models of adaptation at environmental or parapatric margins, and discuss the contrasting effects of migration in either swamping local adaptation, or supplying the genetic variation that is necessary for adaptation to continue. We illustrate how studying adaptation at range margins (both with and without hybridization) can provide insight into the genetic and ecological factors that limit evolution more generally, especially in response to current rates of environmental change.     

Strong genetic differentiation but not local adaptation toward the range limit of a coastal dune plant

All species have limited geographic distributions; but the ecological and evolutionary mechanisms causing range limits are largely unknown. That many species’ geographic range limits are coincident with niche limits suggests limited evolutionary potential of marginal populations to adapt to conditions experienced beyond the range. We provide a test of range limit theory by combining population genetic analysis of microsatellite polymorphisms with a transplant experiment within, at the edge of, and 60 km beyond the northern range of a coastal dune plant. Contrary to expectations, lifetime fitness increased toward the range limit with highest fitness achieved by most populations at and beyond the range edge. Genetic differentiation among populations was strong, with very low, nondirectional gene flow suggesting range limitation via constraints to dispersal. In contrast, however, local adaptation was negligible, and a distance‐dependent decline in fitness only occurred for those populations furthest from home when planted beyond the range limit. These results challenge a commonly held assumption that stable range limits match niche limits, but also raise questions about the unique value of peripheral populations in expanding species’ geographical ranges.     

GENETIC ISOLATION BY ENVIRONMENT OR DISTANCE: WHICH PATTERN OF GENE FLOW IS MOST COMMON?

Gene flow among populations can enhance local adaptation if it introduces new genetic variants available for selection, but strong gene flow can also stall adaptation by swamping locally beneficial genes. These outcomes can depend on population size, genetic variation, and the environmental context. Gene flow patterns may align with geographic distance (IBD—isolation by distance), whereby immigration rates are inversely proportional to the distance between populations. Alternatively gene flow may follow patterns of isolation by environment (IBE), whereby gene flow rates are higher among similar environments. Finally, gene flow may be highest among dissimilar environments (counter‐gradient gene flow), the classic “gene‐swamping” scenario. Here we survey relevant studies to determine the prevalence of each pattern across environmental gradients. Of 70 studies, we found evidence of IBD in 20.0%, IBE in 37.1%, and both patterns in 37.1%. In addition, 10.0% of studies exhibited counter‐gradient gene flow. In total, 74.3% showed significant IBE patterns. This predominant IBE pattern of gene flow may have arisen directly through natural selection or reflect other adaptive and nonadaptive processes leading to nonrandom gene flow. It also precludes gene swamping as a widespread phenomenon. Implications for evolutionary processes and management under rapidly changing environments (e.g., climate change) are discussed.     

Climate structures genetic variation across a species' elevation range: a test of range limits hypotheses

Gene flow may influence the formation of species range limits, and yet little is known about the patterns of gene flow with respect to environmental gradients or proximity to range limits. With rapid environmental change, it is especially important to understand patterns of gene flow to inform conservation efforts. Here we investigate the species range of the selfing, annual plant, Mimulus laciniatus, in the California Sierra Nevada. We assessed genetic variation, gene flow, and population abundance across the entire elevation‐based climate range. Contrary to expectations, within‐population plant density increased towards both climate limits. Mean genetic diversity of edge populations was equivalent to central populations; however, all edge populations exhibited less genetic diversity than neighbouring interior populations. Genetic differentiation was fairly consistent and moderate among all populations, and no directional signals of contemporary gene flow were detected between central and peripheral elevations. Elevation‐driven gene flow (isolation by environment), but not isolation by distance, was found across the species range. These findings were the same towards high‐ and low‐elevation range limits and were inconsistent with two common centre‐edge hypotheses invoked for the formation of species range limits: (i) decreasing habitat quality and population size; (ii) swamping gene flow from large, central populations. This pattern demonstrates that climate, but not centre‐edge dynamics, is an important range‐wide factor structuring M. laciniatus populations. To our knowledge, this is the first empirical study to relate environmental patterns of gene flow to range limits hypotheses. Similar investigations across a wide variety of taxa and life histories are needed.     

Genetic diversity and structuring across the range of a widely distributed ladybird: focus on rear‐edge populations phenotypically divergent

Population genetics and phenotypic structures are often predicted to vary along the geographic range of a species. This phenomenon would be accentuated for species with large range areas, with discontinuities and marginal populations. We herein compare the genetic patterns of central populations of Coccinella septempunctata L. with those of two phenotypically differentiated populations considered as rear‐edge populations and subspecies based on phenotype (Algeria and Japan). According to the central‐marginal model and expected characteristics of rear‐edge populations, we hypothesize that these rear‐edge populations have (1) a reduced genetic diversity, resulting from their relative isolation over long periods of time, (2) a higher population genetic differentiation, explained by low contemporary gene flow levels, and (3) a relationship between genetic diversity characteristics and phenotypes, due to historical isolation and/or local adaptation. Based on genotyping of 28 populations for 18 microsatellite markers, several levels of regional genetic diversity and differentiation are observed between and within populations, according to their localization: low within‐population genetic diversity and higher genetic differentiation of rear‐edge populations. The genetic structuring clearly dissociates the Algerian and Eastern Asia populations from the others. Geographical patterns of genetic diversity and differentiation support the hypothesis of the central‐marginal model. The pattern observed is in agreement with the phenotypic structure across species range. A clear genetic break between populations of Algeria, the Eastern Asia, and the remaining populations is a dominant feature of the data. Differential local adaptations, absence of gene flow between marginal and central populations, and/or incapacity to mate after colonization, have contributed to their distinct genotypic and phenotypic characteristics.     

Barriers to sympatry between avian sibling species (Paridae: Baeolophus) in local secondary contact

Range limits and secondary contact zones often occur at ecotones between major associations of habitat and climate. Therefore, understanding processes that limit sympatry between species in such areas provides an important framework for testing biogeographic and evolutionary hypotheses. Theoretical and empirical work has shown that the evolution of species borders is influenced by a complexity of factors, including gene flow from central to peripheral populations and the ability of species to adapt locally to environmental conditions. However, few studies have used bioclimatic models, combined with molecular and morphological data, to predict geographic range limits in the context of gene flow across a secondary contact zone. In this study, I applied these methods to test specific hypotheses about barriers to sympatry between closely related species where they approach and contact each other. Specifically, I examined the importance of historical isolation, local adaptation, and symmetry of gene flow in limiting sympatry and range expansion of ecologically distinct species across environmental gradients. Molecular (mitochondrial DNA, allozymes), morphological, and bioclimatic data were obtained for two avian sibling species (Baeolophus inornatus and B. ridgwayi) that exist in recent, narrow secondary contact in northern California. These species are broadly allopatric and occupy rangewide associations of oak and pinyon-juniper woodlands, respectively, although B. inornatus also inhabits mixed or juniper woodlands locally. Patterns of molecular variation generally were congruent with morphological and bioclimatic data, and support prior evidence for a history of isolation, adaptation, and divergence in distinctive, species-specific vegetation-climate associations. However, molecular and morphological clines fall east of the limit of oaks, and individuals of B. inornatus in this juniper-associated contact zone experience bioclimates that are more similar to B. ridgwayi than to B. inornatus in oak habitat. Thus, B. inornatus is able to adapt and expand locally into the range of its close relative, but not vice versa. These data support the hypothesis that gene flow is asymmetrical where peripheral populations meet at range boundaries. Physiological differences between species may play an important role in influencing these patterns. Empirical studies that highlight the importance of local adaptation and patterns of gene flow in which closely related species contact across ecotones are central to understanding limits on geographic ranges, sympatry, and introgression-a cornerstone of biogeographic and speciation theory.     

Efficient long-distance gene flow into an isolated relict oak stand

Geographically isolated and small populations outside a species' central distribution range are likely to be of major importance to a species' ability to quickly adjust its distribution range to global change dynamics. Gene flow from the outside plays a pivotal role in the fate of these marginal populations. It has been proposed that spatial fragmentation and perceived geographic isolation do not necessarily reflect a loss of genetic connectivity in tree species. However, the spatial limits of long-distance gene flow, as well as its magnitude and impact, are still generally unknown. In the present study, we analyzed long-distance pollen-mediated gene flow into an isolated relict stand consisting of 7 individuals of Quercus robur L. based on a total sample of 177 trees and 9 microsatellite loci. We show that pollen-mediated gene flow across more than 80 km in this wind-pollinated tree species contributed at least 35% of all successful pollinations in the investigated isolated and small oak stand at the eastern limit of the species' distribution. The observed pollen immigration shaped the genetic diversity of acorn progenies in the stand and might explain the comparably high genetic diversity in the persisting adult population.     

Population genetics and the evolution of geographic range limits in an annual plant

Abstract Theoretical models of species' geographic range limits have identified both demographic and evolutionary mechanisms that prevent range expansion. Stable range limits have been paradoxical for evolutionary biologists because they represent locations where populations chronically fail to respond to selection. Distinguishing among the proposed causes of species' range limits requires insight into both current and historical population dynamics. The tools of molecular population genetics provide a window into the stability of range limits, historical demography, and rates of gene flow. Here we evaluate alternative range limit models using a multilocus data set based on DNA sequences and microsatellites along with field demographic data from the annual plant Clarkia xantiana ssp. xantiana. Our data suggest that central and peripheral populations have very large historical and current effective population sizes and that there is little evidence for population size changes or bottlenecks associated with colonization in peripheral populations. Whereas range limit populations appear to have been stable, central populations exhibit a signature of population expansion and have contributed asymmetrically to the genetic diversity of peripheral populations via migration. Overall, our results discount strictly demographic models of range limits and more strongly support evolutionary genetic models of range limits, where adaptation is prevented by a lack of genetic variation or maladaptive gene flow.     

Local adaptations to frost in marginal and central populations of the dominant forest tree Fagus sylvatica L. as affected by temperature and extreme drought in common garden experiments

Local adaptations to environmental conditions are of high ecological importance as they determine distribution ranges and likely affect species responses to climate change. Increased environmental stress (warming, extreme drought) due to climate change in combination with decreased genetic mixing due to isolation may lead to stronger local adaptations of geographically marginal than central populations. We experimentally observed local adaptations of three marginal and four central populations of Fagus sylvatica L., the dominant native forest tree, to frost over winter and in spring (late frost). We determined frost hardiness of buds and roots by the relative electrolyte leakage in two common garden experiments. The experiment at the cold site included a continuous warming treatment; the experiment at the warm site included a preceding summer drought manipulation. In both experiments, we found evidence for local adaptation to frost, with stronger signs of local adaptation in marginal populations. Winter frost killed many of the potted individuals at the cold site, with higher survival in the warming treatment and in those populations originating from colder environments. However, we found no difference in winter frost tolerance of buds among populations, implying that bud survival was not the main cue for mortality. Bud late frost tolerance in April differed between populations at the warm site, mainly because of phenological differences in bud break. Increased spring frost tolerance of plants which had experienced drought stress in the preceding summer could also be explained by shifts in phenology. Stronger local adaptations to climate in geographically marginal than central populations imply the potential for adaptation to climate at range edges. In times of climate change, however, it needs to be tested whether locally adapted populations at range margins can successfully adapt further to changing conditions.     

Adaptation to an invasive host is driving the loss of a native ecotype

Locally adapted populations are often used as model systems for the early stages of ecological speciation, but most of these young divergent populations will never become complete species. The maintenance of local adaptation relies on the strength of natural selection overwhelming the homogenizing effects of gene flow; however, this balance may be readily upset in changing environments. Here I show that soapberry bugs (Jadera haematoloma) have lost adaptations to their native host plant (Cardiospermum corindum) and are regionally specializing on an invasive host (Koelreuteria elegans), collapsing a classic and well‐documented example of local adaptation. All populations that were adapted to the native host—including those still found on that host today—are now better adapted to the invasive host in multiple phenotypes. Weak differentiation remains in two traits, suggesting that homogenization across the region is incomplete. This study highlights the potential for adaptation to invasive species to disrupt native communities by swamping adaptation to native conditions through maladaptive gene flow.     

Theoretical perspectives on the statics and dynamics of species' borders in patchy environments

Understanding range limits is a fundamental problem in ecology and evolutionary biology. In 1963, Mayr argued that "contaminating" gene flow from central populations constrained adaptation in marginal populations, preventing range expansion, while in 1984, Bradshaw suggested that absence of genetic variation prevented species from occurring everywhere. Understanding stability of range boundaries requires unraveling the interplay of demography, gene flow, and evolution of populations in concrete landscape settings. We walk through a set of interrelated spatial scenarios that illustrate interesting complexities of this interplay. To motivate our individual-based model results, we consider a hypothetical zooplankter in a landscape of discrete water bodies coupled by dispersal. We examine how patterns of dispersal influence adaptation in sink habitats where conditions are outside the species' niche. The likelihood of observing niche evolution (and thus range expansion) over any given timescale depends on (1) the degree of initial maladaptation; (2) pattern (pulsed vs. continuous, uni- vs. bidirectional), timing (juvenile vs. adult), and rate of dispersal (and hence population size); (3) mutation rate; (4) sexuality; and (5) the degree of heterogeneity in the occupied range. We also show how the genetic architecture of polygenic adaptation is influenced by the interplay of selection and dispersal in heterogeneous landscapes.     

Potential for adaptive evolution at species range margins: contrasting interactions between red coral populations and their environment in a changing ocean

Studying population‐by‐environment interactions (PEIs) at species range margins offers the opportunity to characterize the responses of populations facing an extreme regime of selection, as expected due to global change. Nevertheless, the importance of these marginal populations as putative reservoirs of adaptive genetic variation has scarcely been considered in conservation biology. This is particularly true in marine ecosystems for which the deep refugia hypothesis proposes that disturbed shallow and marginal populations of a given species can be replenished by mesophotic ones. This hypothesis therefore assumes that identical PEIs exist between populations, neglecting the potential for adaptation at species range margins. Here, we combine reciprocal transplant and common garden experiments with population genetics analyses to decipher the PEIs in the red coral, Corallium rubrum. Our analyses reveal partially contrasting PEIs between shallow and mesophotic populations separated by approximately one hundred meters, suggesting that red coral populations may potentially be locally adapted to their environment. Based on the effective population size and connectivity analyses, we posit that genetic drift may be more important than gene flow in the adaptation of the red coral. We further investigate how adaptive divergence could impact population viability in the context of warming and demonstrate differential phenotypic buffering capacities against thermal stress. Our study questions the relevance of the deep refugia hypothesis and highlights the conservation value of marginal populations as a putative reservoir of adaptive genetic polymorphism.     

Consequences of recurrent gene flow from crops to wild relatives

Concern about gene flow from crops to wild relatives has become widespread with the increasing cultivation of transgenic crops. Possible consequences of such gene flow include genetic assimilation, wherein crop genes replace wild ones, and demographic swamping, wherein hybrids are less fertile than their wild parents, and wild populations shrink. Using mathematical models of a wild population recurrently receiving pollen from a genetically fixed crop, we find that the conditions for genetic assimilation are not stringent, and progress towards replacement can be fast, even for disfavoured crop genes. Demographic swamping and genetic drift relax the conditions for genetic assimilation and speed progress towards replacement. Genetic assimilation can involve thresholds and hysteresis, such that a small increase in immigration can lead to fixation of a disfavoured crop gene that had been maintained at a moderate frequency, even if the increase in immigration is cancelled before the gene fixes. Demographic swamping can give rise to 'migrational meltdown', such that a small increase in immigration can lead to not only fixation of a disfavoured crop gene but also drastic shrinkage of the wild population. These findings suggest that the spread of crop genes in wild populations should be monitored more closely.     

Spatial variation in climate mediates gene flow across an island archipelago

High levels of gene flow among partially isolated populations can overwhelm selection and limit local adaptation. This process, known as “gene swamping,” can homogenize genetic diversity among populations and reduce the capacity of a species to withstand rapid environmental change. We studied brown anole lizards (Anolis sagrei) distributed across seven islands in The Bahamas. We used microsatellite markers to estimate gene flow among islands and then examined the correlation between thermal performance and island temperature. The thermal optimum for sprint performance was correlated with both mean and maximum island temperature, whereas performance breadth was not correlated with any measure of temperature variation. Gene flow between islands decreased as the difference between mean island temperatures increased, even when those islands were adjacent to one another. These data suggest that phenotypic variation is the result of either (1) local genetic adaptation with selection against immigrants maintaining variation in the thermal optimum, (2) irreversible forms of adaptive plasticity such that immigrants have reduced fitness, or (3) an interaction between fixed genetic differences and plasticity. In general, the patterns of gene flow we observed suggest that local thermal environments represent important ecological filters that can mediate gene flow on relatively fine geographic scales.     

Divergent selection and heterogeneous migration rates across the range of Sitka spruce (Picea sitchensis)

Gene flow and effective population size (N(e)) should depend on a population's position within its range: those near the edges are expected to have smaller N(e) and lower relative emigration rates, whereas those nearer the centre should have larger N(e) and higher relative emigration rates. In species with continuous ranges, this phenomenon may limit the ability of peripheral populations to respond to divergent selection. Here, we employ Sitka spruce as a model to test these predictions. We previously genotyped 339 single nucleotide polymorphisms (SNPs) in 410 individuals from 13 populations, and used these data to identify putative targets of divergent selection, as well as to explore the extent to which central-peripheral structure may impede adaptation. Fourteen SNPs had outlier F(ST) estimates suggestive of divergent selection, of which nine were previously associated with phenotypic variation in adaptive traits (timing of autumn budset and cold hardiness). Using coalescent simulations, we show that populations from near the centre of the range have higher effective populations sizes than those from the edges, and that central populations contribute more migrants to marginal populations than the reverse. Our results suggest that while divergent selection appears to have shaped allele frequencies among populations, asymmetrical movement of alleles from the centre to the edges of the species range may affect the adaptive capacity of peripheral populations. In southern peripheral populations, the movement of cold-adapted alleles from the north represents a significant impediment to adaptation under climate change, while in the north, movement of warm-adapted alleles from the south may enhance adaptation.     

The evolution of species' distributions: reciprocal transplants across the elevation ranges of Mimulus cardinalis and M. lewisii

Every species occupies a limited geographic area, but it remains unclear why traits that limit distribution do not evolve to allow range expansion. Hypotheses for the evolutionary stability of geographic ranges assume that species are maladapted at the range boundary and unfit beyond the current range, but this assumption has rarely been tested. To examine how fitness varies across species' ranges, we reciprocally transplanted two species of monkeyflowers, Mimulus cardinalis and M. lewisii, within and beyond their present elevation ranges. We used individuals of known parentage from populations collected across the elevation ranges of both species to examine whether populations are adapted to position within the range. For both species we found the greatest average fitness at elevations central within the range, reduced fitness at the range margin, and zero or near-zero fitness when transplanted beyond their present elevation range limits. However, the underlying causes of fitness variation differed between the species. At high elevations beyond its range, M. cardinalis displayed reduced growth and fecundity, whereas at low elevations M. lewisii experienced high mortality. Weak differences in performance were observed among populations within each species and these were not related to elevation of origin. Low fitness of both species at their range margin and weak differentiation among populations within each species suggest that adaptation to the environment at and beyond the range margin is hindered, illustrating that range margins provide an interesting system in which to study limits to adaptation.     

Genetic diversity across the range of a temperate lizard

Aim  To examine range-wide patterns of genetic diversity in association with range limits in a broadly distributed temperate lizard, and to identify the contributions of a series of environmental, geographical and historical variables to the observed patterns. Reduced genetic diversity may limit local adaptation in peripheral populations, thereby limiting their ability to adapt to marginal environmental conditions, possibly explaining the existence of temporally stable range limits.
Location  Various sampling locales throughout eastern and central USA and southern Ontario, Canada.
Methods  Genetic diversity of nuclear DNA microsatellites was estimated for each of 38 populations from across the range of eastern North America's most broadly distributed lizard, the five-lined skink, Plestiodon fasciatus (Linnaeus, 1758).
Results  Local climatic conditions and an interaction between distance from range border and glaciation history best predicted a population's present-day genetic diversity. Overall, peripheral populations had reduced genetic diversity relative to that of central populations, but this difference was attributable to the reduced genetic diversity in peripheral populations to the north and west that are not bordered by any obvious physical boundaries.
Main conclusions  Some, but not all, peripheral populations had reduced genetic diversity relative to that of more central populations, which probably arose through an interaction of ecological and historical factors. Peripheral populations that were bordered by an obvious boundary (e.g. an ocean) had higher diversity than peripheral populations that were not bordered by an obvious physical barrier to range expansion, suggesting that reduced intrapopulation genetic diversity is associated with range limits in the five-lined skink.     

Local adaptation at range edges: comparing elevation and latitudinal gradients

Local adaptation at range edges influences species’ distributions and how they respond to environmental change. However, the factors that affect adaptation, including gene flow and local selection pressures, are likely to vary across different types of range edge. We performed a reciprocal transplant experiment to investigate local adaptation in populations of Plantago lanceolata and P. major from central locations in their European range and from their latitudinal and elevation range edges (in northern Scandinavia and Swiss Alps, respectively). We also characterized patterns of genetic diversity and differentiation in populations using molecular markers. Range‐centre plants of P. major were adapted to conditions at the range centre, but performed similarly to range‐edge plants when grown at the range edges. There was no evidence for local adaptation when comparing central and edge populations of P. lanceolata. However, plants of both species from high elevation were locally adapted when compared with plants from high latitude, although the reverse was not true. This asymmetry was associated with greater genetic diversity and less genetic differentiation over the elevation gradient than over the latitudinal gradient. Our results suggest that adaptation in some range‐edge populations could increase their performance following climate change. However, responses are likely to differ along elevation and latitudinal gradients, with adaptation more likely at high‐elevation. Furthermore, based upon these results, we suggest that gene flow is unlikely to constrain adaptation in range‐edge populations of these species.     

Extremely low genetic diversity and extensive genetic admixture at the northern range margins of Bombax ceiba

Understanding the evolutionary processes in species at the margins of their range is of great significance, because marginal populations may harbor local adaptations and will initiate further expansion in response to changes in the environment. Here we examined genetic variation in two nuclear genes and one chloroplast intergenic spacer in 13 northern marginal populations and one geographically central population of Bombax ceiba, a tree distributed mainly in tropical regions. Our results revealed an extremely low level of genetic diversity in each population at the northern margin of its range and strong genetic differentiation between southern China and South Asia. Cultivated and natural populations showed no significant differences in genetic variability. Genetic admixture in a nuclear gene was detected in 10 of the 13 populations at the northern margin of their range. The founder effect, in which a small number of individuals colonize the northern margins of its range, may explain the extremely low genetic diversity. During the establishment of new populations, different source populations may mix and undergo further genetic drift and differentiation. This study indicates that patterns of genetic diversity in tropical species at the margin of their range may also be severely influenced by founder effects.